Abstract
The distribution of carbohydrate moieties in lancelet (Branchiostoma belcheri) oocytes has been studied at different stages of development, using a peroxidase-labeled lectin incubation technique, the PAS-reaction and Alcian Blue staining. Binding sites of 5 lectins, indicating the presence of different sugar moieties (Wheat germ agglutinin (WGA) for N-acetylglucosamine, Concanavalin A (Con A) for glucose/mannose, Helix pomatia agglutinin (HPA) for N-acetyl-D-galactosamine, Ricinus communis agglutinin (RCA-I) for galactose and Ulex europaeus agglutinin (UEA-I) for fucose), were identified and were shown to undergo considerable variation during oocyte development. In the previtellogenic stage, HPA, RCA-I and UEA-I were not identified on the oocyte surface, but WGA and Con A gave strongly positive reactions at this site. In the cytoplasm, 4 lectins (Con A, HPA, RCA-I and UEA-I) gave a weak or moderate reaction, and Con A was also observed in the perinuclear region. In vitellogenic oocytes, these 4 lectins were found to also bind to the nuclear envelope, karyoplasm and nucleolus, and, with the exception of Con A, could also be found in the nuclei of more mature stages. The cytoplasmic yolk granules and Golgi vesicles of the vitellogenic oocyte, were moderately positive for Con A, HPA, RCA-I and UEA-I, but HPA, RCA-I and UEA-I were only weakly bound at the oocyte surface. In mature oocytes, all 5 lectins bound moderately or strongly to yolk granules and cell surface. HPA, RCA-I and UEA-I bound moderately or strongly to various nuclear compartments. Thus, carbohydrate content varied with the development and maturation of the oocytes, and the PAS results were in agreement with the lectin-binding results. Charged carbohydrate residues were observed in the egg envelope and Golgi bodies.
These results suggest that the appearence of Con A-, HPA-, RCA-I- and UEA-I-binding glycoconjugates in the nuclei of developing oocytes show a varying pattern indicating different phases of nuclear activity which correlate with different carbohydrate synthetic activities of the oocyte.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Araujo ACG, Souto-Padron T, Souza W de (1993) Cytochemical localization of carbohydrate residues in microfariae of Wuchereria bancrofti and Brugia malayi. Cytochemistry 41:571–578
Chang CY, Zhu YT, Cheng DY (1982) Immunocytochemical demonstration of luteinizing hormone (LH) in Hatschek's pit of amphioxus (Branchiostoma belcheri Gray). Kexue Tongbao 27:1233–1234
Chang CY, Liu YH, Zhu HH (1985) Steroid hormones and their functional regulation in amphioxus. In: Lofts B, Holmes WN (eds) Current trends in comparative endocrinology. Hong Kong University Press, Hong Kong, pp 205–207
Chou Ch-F, Omary MB (1994) Mitotic arrest with anti-microtubule agents or okadaic acid is associated with increased glucoprotein terminal GlcNAc's. J Cell Sci 107:1833–1843
Contin A, Falugi C, Fasulo S (1992) Developmental regulation of lectin-binding patterns in Paracentrotus lividus gonads, gametes and early embryos. Acta Histochem 92:179–189
Debray H, Decout D, Strecher G, Spik G, Montreuil J (1981) Specificity of twelve lectins towards oligosaccharides and glycopeptides related to N-glycosylproteins. Eur J Biochem 117:41–46
Fang YQ (1991) New demonstrations on a regulatory system of reproductive hormone in amphioxus (Branchiostoma belcheri Gray). In: Saxena RN, Muralidhar K, Bhagat L, Sehgat N, Saxena T, Kaushal P (eds) Current themes in comparative endocrinology. Delhi University Press, Delhi, p 148
Fang YQ, Qi X (1989) Ultrastructural study of the Hatschek's pit epithelial cell of amphioxus. Science in China (Series B) 32:1465–1472
Fang YQ, Qi X (1990) Process of oogenesis in amphioxus. J Oceanography in Taiwan Strait 9:375–380
Fang YQ, Qi X (1992) Ultrastructural study of oogenesis of amphioxus in Xiamen. Acta Oceanologica Sinica 9:579–589
Fang YQ, Qi X, Liamp P, Hong GY (1991) Annual change of the gonadal development of amphioxus in Xiamen. Acta Oceanologica Sinica 10:477–480
Fang YQ, Zhao WX, Wei H (1993) Correlative study of level of steroid hormone with gonadal development. Chinese Science Bulletin 38:1290–1294
Fang YQ, Zhao WX, Lin QM (1993) The study of hormonal regulation on the oocyte development and maturation of amphioxus. (Chinese plate; English plate in press.) Science in China (Series B) 23:612–161
Foltz KR, Lennarz WJ (1990) Purification and characterization of an extracellular fragment of the sea urchin egg receptor for sperm. J Cell Biology 111:2951–2959
Glabe CG, Grabel LB, Vacqier VD, Rosen SD (1982) Carbohydrate specificity of sea urchin sperm binding: a cell surface lectin mediating sperm-egg interation. J Cell Biology 94:123–128
Goldstein IJ, Poretz RD (1986) Isolation, physicochemical characterization and carbohydrate-binding specificity of lectins. In: Liener IE, Sharon N, Goldstein IJ (eds) The lectins. Academic Press, Orlando, FL, p 33
Guraya SS (1983) Reproductive biology of invertebrate, vol I. In: Adiyodi KG, Adiyodi RG (eds) Oogenesis, oviposition and oosorotion. Wiley, New York, pp 735–752
Hammarström S, Murghy LA, Goldstein IJ, Etzler ME (1977) Carbohydrate binding specificity of four N-acetyl-D-galactosamine-“specific” lectins: Helix pomatia A hemagglutinin, Soybean agglutinin, Lima bean lectin, and Dolichos biflorus lectin. Biochemistry 16:2750–2755
Holland ND, Holland LZ (1991) The fine structure of the growth stage oocytes of a lancelet (=amphioxus), Branchiostoma lanceolatum. Invertebrate Reproduction and Development 19:107–122
Horvat B (1993) Galactose-binding lectins as markers of pregnancy-related glycoproteins. Histochemistry 99:95–101
Koch EA, Spitzer RH (1982) Autoradiographic studies of protein and polysaccharide synthesis during vitellogenesis in Drosophila. Cell Tissue Res 224:315–333
Lev R, Spicer SS (1964) Specific staining of sulfate groups with alcian blue at low pH. J Histochem Cytochem 12, 309
Meiniel R, Molatz J-L, Meiniel A (1986) Concanavalin A-binding glycoproteins in the subcommissural and pineal organ of the sheep (Ovis aries). A fluorescence-microscopic and electrophoretic study. Cell Tissue Res 245:605–613
Murata H, Takahashi N, Yamada K (1984) Effects of digestion with N-oligosaccharide glycopeptidase upon certain lectinperoxidase-diaminbenzidine reactions of glycoproteins in mammalian and avian tissues. Histochemistry 81:401–407
Nozaki M, Gorbman A (1992) The question of functional homology of Hatschek's pit of amphioxus (Branchiostoma belcheri) and the vertebrate adenohypophysis. Zoological Science 9:287–295
Romeis B (1989) Mikroskopische Technik, 16 edn. Urban & Schwarzenberg, München Wien
Schreibman MP, Demski SS, Margolis-Nunno H (1986) Immunoreactive (ir-) LHRH in the “brain” of amphioxus. (abstract) Amer Zool 26:30A
Schmell E, Earles BJ, Breaux C, Lennarz WJ (1977) Identification of a sperm receptor on the surface of the egg of the sea urchin Arbacia punctuata. J Cell Biol 72:35–46
Song YC, Xu MQ (1989) Reproductive biology of amphioxus in Qingtau: I the observation of oocyte development and ovary. Oceanic Science 4:50–54
Spicer SS, Horn RC, Leppi TJ (1967) Histochemistry of connective tissue mucopolysaccharides. In: Wagner BM, Smith DE (eds) The connective tissue. Williams & Wilkins, Baltimore, pp 251–276
Spicer SS, Schulte BA (1992) Diversity of cell glycoconjugates shown histochemically: a perspective. J Histochemistry Cytochemistry 40:1–38
Storch V, Welsch U (1991) Systematische Zoologie, 4th edn. Fischer, Stuttgart
Sugii S, Kabat EA, Baer HH (1982) Further immunochemical studies on the combining sites of Lotus tetragonolobus and Ulex europaeus I and II lectins. Carbohydrate Res 99:99–105
Wang DH, Wang DY (1987) Preliminary study on correlation of oocyte organelle with vitellogenesis of amphioxus in Xiamen. Acta Xiamen University (Natural Science plate) 26:615–619
Wassarman P (1989) Role of carbohydrates in receptormediated fertilization in mammals. Carbohydrate recognition in cellular function. (Ciba Foundation Symposium 145) Wiley, Chichester pp 135–155
Welsch U, Schumacher U (1986) Carbohydrate histochemistry of two tunicate species (Ciona intestinalis and Dendrodoa grossularia). Zool Jb 114:69–81
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Fang, Y.Q., Welsch, U. A histochemical study of the distribution of lectin binding sites in the developing oocytes of the lancelet Branchiostoma belcheri . Cell Tissue Res 280, 427–434 (1995). https://doi.org/10.1007/BF00307816
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00307816